Vertebrate LTR Retrotransposons of the Tf1/Sushi Group

Butler, Margaret I.; Goodwin, Timothy J. D.; Simpson, Matthew A.; Singh, Monica; Poulter, Russell T. M.

doi:10.1007/s002390010154

Cited by 51 publications

(67 citation statements)

References 45 publications

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“…This gene was designated as AoLTR. In addition, similar to the situation in some LTR retroelements (Butler et al, 2001), it was predicted that the shift in transcription from ORF 1 to ORF 2 occurred by a-1 frameshift in AFLAV (Hua et al, 2007). Alignment of the deduced amino acid sequence of the AoLTR gene showed 94% overall identity with that of the A. flavus AFLAV whole sequence, which contains ORF 1 and ORF 2 (Fig.…”

Section: Discovery Of Multiple Copies Of a Putative Ltr-retrotranspossupporting

confidence: 62%

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Discovery and analysis of an active long terminal repeat-retrotransposable element in Aspergillus oryzae

Jin

Hara

Sato

et al. 2014

J. Gen. Appl. Microbiol.

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Wild-type Aspergillus oryzae RIB40 contains two copies of the AO090005001597 gene. We previously constructed A. oryzae RIB40 strain, RKuAF8B, with multiple chromosomal deletions, in which the AO090005001597 copy number was found to be increased significantly. Sequence analysis indicated that AO090005001597 is part of a putative 6,000-bp retrotransposable element, flanked by two long terminal repeats (LTRs) of 669 bp, with characteristics of retroviruses and retrotransposons, and thus designated AoLTR (A. oryzae LTR-retrotransposable element). AoLTR comprised putative reverse transcriptase, RNase H, and integrase domains. The deduced amino acid sequence alignment of AoLTR showed 94% overall identity with AFLAV, an A. flavus Tf1/sushi retrotransposon. Quantitative realtime RT-PCR showed that AoLTR gene expression was significantly increased in the RKuAF8B, in accordance with the increased copy number. Inverse PCR indicated that the full-length retrotransposable element was randomly integrated into multiple genomic locations. However, no obvious phenotypic changes were associated with the increased AoLTR gene copy number.

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Section: Discovery Of Multiple Copies Of a Putative Ltr-retrotranspossupporting

confidence: 62%

“…Among these, the Ty3/gypsy group of LTR retrotransposons has been found in a wide range of filamentous fungi, and Tf1/sushi represents a subgroup of the Ty3/gypsy family (Butler et al, 2001). Although some fungal LTR-retrotransposons have been reported, their ability to transpose has rarely been proven.…”

Section: Introductionmentioning

confidence: 99%

Discovery and analysis of an active long terminal repeat-retrotransposable element in Aspergillus oryzae

Jin

Hara

Sato

et al. 2014

J. Gen. Appl. Microbiol.

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“…From the time when a self-priming mechanism was suggested for Tf1, a similar priming mechanism has also been proposed for several LTR retroelements, such as the highly homologous Tf2 and Maggy, Skippy, Cft-1, Boty, copia of maize, and Tf1/shushi of vertebrates, which all belong to a single lineage of the T3/gypsy group of LTR retrotransposons (5,7,21). These elements are believed to have diverged early in the evolution of LTR retrotransposons, well before retroviruses.…”

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confidence: 88%

The Reverse Transcriptase of the Tf1 Retrotransposon Has a Specific Novel Activity for Generating the RNA Self-Primer That Is Functional in cDNA Synthesis

Hizi

2008

J Virol

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The Tf1 retrotransposon of Schizosaccharomyces pombe represents a group of eukaryotic long terminal repeat (LTR) retroelements that, based on their sequences, were predicted to use an RNA self-primer for initiating reverse transcription while synthesizing the negative-sense DNA strand. This feature is substantially different from the one typical to retroviruses and other LTR retrotransposons that all exhibit a tRNA-dependent priming mechanism. Genetic studies have suggested that the self-primer of Tf1 can be generated by a cleavage between the 11th and 12th bases of the Tf1 RNA transcript. The in vitro data presented here show that recombinant Tf1 reverse transcriptase indeed introduces a nick at the end of a duplexed region at the 5 end of Tf1 genomic RNA, substantiating the prediction that this enzyme is responsible for generating this RNA self-primer. The 3 end of the primer, generated in this manner, can then be extended upon the addition of deoxynucleoside triphosphates by the DNA polymerase activity of the same enzyme, synthesizing the negativesense DNA strand. This functional primer must have been generated by the RNase H activity of Tf1 reverse transcriptase, since a mutant enzyme lacking this activity has lost its ability to generate the self-primer. It was also found here that the reverse transcriptases of human immunodeficiency virus type 1 and of murine leukemia virus do not exhibit this specific cleavage activity. In all, it is likely that the observed unique mechanism of self-priming in Tf1 represents an early advantageous form of initiating reverse transcription in LTR retroelements without involving cellular tRNAs.Long terminal repeat (LTR) retrotransposons are retrovirus-like elements found in a broad variety of eukaryotic cells (6,7,10). Their structure and mechanisms of propagation are related to retroviruses, and like them, they encode the Gag, protease, reverse transcriptase (RT), and integrase proteins. As with all retroviruses, the RTs of LTR retrotransposons are pivotal for converting the positive-sense, single-stranded RNA genome into a double-stranded and integration-competent viral DNA. This reverse transcription (RTN) process is catalyzed by two RT activities, DNA polymerase activity, which copies both RNA and DNA, and RNase H activity, which concomitantly cleaves the RNA in the DNA-RNA heteroduplex formed. In all retroviruses and LTR retrotransposons, the synthesis of negative-strand DNA is initiated from an RNA primer that is complementary to a specific genomic RNA sequence, the primer binding site (PBS), which is located near the 5Ј end of the RNA genome. It is well documented that this RNA primer is a specific cellular tRNA (for examples, see references 6, 7, 16, and 27).Interestingly, an alternative tRNA-independent priming mechanism was proposed for the LTR retrotransposon Tf1 of the fission yeast Schizosaccharomyces pombe by . This model suggests that a self-complementarity within the RNA genome allows intramolecular base pairing near the 5Ј end of the RNA, causing this end to ...

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“…Instead of using a tRNA, Tf1 primes minus-strand synthesis with an 11-nucleotide RNA removed from the 5Ј end of its own transcript. An increasing number of LTR elements in eukaryotes from yeast to vertebrates are found to use this self-priming mechanism (3,16).…”

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confidence: 99%

The Self Primer of the Long Terminal Repeat Retrotransposon Tf1 Is Not Removed during Reverse Transcription

Atwood-Moore

Yan

Judson

et al. 2006

J Virol

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The long terminal repeat retrotransposon Tf1 of Schizosaccharomyces pombe uses a unique mechanism of self priming to initiate reverse transcription. Instead of using a tRNA, Tf1 primes minus-strand synthesis with an 11-nucleotide RNA removed from the 5 end of its own transcript. We tested whether the self primer of Tf1 was similar to tRNA primers in being removed from the cDNA by RNase H. Our analysis of Tf1 cDNA extracted from virus-like particles revealed the surprising observation that the dominant species of cDNA retained the self primer. This suggests that integration of the cDNA relies on mechanisms other than reverse transcription to remove the primer.The reverse transcription of retroviruses and long terminal repeat (LTR) retrotransposons is primed by specific tRNA species for minus-strand initiation and by polypurine tracts (PPT) for plus-strand initiation. These primers play a critical role in defining the ends of the cDNA such that the "CA" dinucleotides required for integration are positioned at the termini (23). During reverse transcription the RNase H activity of reverse transcriptase (RT) removes the tRNA and PPT primers from the 5Ј ends of the cDNA so that their sequences are not copied into the 3Ј termini of the complementary strand of cDNA. This is a critical feature of reverse transcription because addition of these nucleotides after the conserved "CA" at the 3Ј ends of the cDNA would block integration.The LTR retrotransposon Tf1 of Schizosaccharomyces pombe uses a unique mechanism of self priming to initiate reverse transcription (11)(12)(13)15). Instead of using a tRNA, Tf1 primes minus-strand synthesis with an 11-nucleotide RNA removed from the 5Ј end of its own transcript. An increasing number of LTR elements in eukaryotes from yeast to vertebrates are found to use this self-priming mechanism (3, 16).A recent study of mutations in the RT of Tf1 revealed that RNase H removes the PPT from the 5Ј end of the plus-strand cDNA (2). Random mutagenesis of RT resulted in a cluster of mutations in RNase H that inhibited the removal of the PPT without reducing the amount of cDNA produced. That RNase H was responsible for primer removal was not surprising because the PPT of Tf1 is similar to those of other LTR elements. However, because of its unique nature, it is not known whether the self primer of Tf1 is also removed by RNase H.To determine whether the self primer of Tf1 was removed during reverse transcription, we sequenced the ends of cDNA produced by the plasmid copy of Tf1 (Tf1-neoAI) used for transposition assays (1, 11). Virus-like particles were isolated from cultures of S. pombe (YHL6742) and purified on sucrose gradients, and cDNA was extracted (11,14). We determined the sequence of the cDNA at the 3Ј end of the plus strand by ligating an oligonucleotide to the cDNA and using a complementary oligonucleotide to amplify by PCR the terminal sequences (Fig. 1). A ligation bias that could alter the sequence data obtained with this technique has not been observed (18). The ligation-mediated PCR ...

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Vertebrate LTR Retrotransposons of the Tf1/Sushi Group

Cited by 51 publications

References 45 publications

Discovery and analysis of an active long terminal repeat-retrotransposable element in Aspergillus oryzae

Discovery and analysis of an active long terminal repeat-retrotransposable element in Aspergillus oryzae

The Reverse Transcriptase of the Tf1 Retrotransposon Has a Specific Novel Activity for Generating the RNA Self-Primer That Is Functional in cDNA Synthesis

The Self Primer of the Long Terminal Repeat Retrotransposon Tf1 Is Not Removed during Reverse Transcription

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